Discussion
Costly sexually selected traits may affect viability, especially in
stressful environments, and it has long been speculated that, for
example, Irish elk (Megaloceros giganteus ), characterized by
extremely elaborated antlers, went extinct when glaciation limited
resource availability (Moen et al., 1999; but see O’Driscoll Worman &
Kimbrell, 2008). However, the effect of elaborated sexual traits on
extinction risk remains unresolved, with comparative analyses yielding
conflicting results (Doherty et al., 2003; Morrow & Pitcher, 2003;
Martins et al., 2018; Parrett et al., 2019). Our study is the first
experimental evidence showing that during the environmental change, the
presence of elaborated sexual trait in a population elevates the risk of
extinction.
Our results contrast with those obtained by manipulating opportunity
sexual selection via mating system and sex ratio, which generally find
positive effect of sexual selection on fitness correlates (reviewed in
Cally et al., 2019) and population survival (Jarzebowska & Radwan,
2010; Plesnar-Bielak et al., 2012; but see Parrett and Knell 2018). This
apparent inconsistency can be reconciled by conceptually separating
short-term from long term impacts of sexual selection (Figure 3). In the
short timescale, the effects of sexual and natural selection act on
phenotypic variation present in a population at a given point in time.
Under condition-dependence, both types of selection can to a large
extent be aligned, especially during environmental change (Long et al.,
2012; Plesnar-Bielak et al., 2012; Parrett & Knell, 2018). However, in
the long term, as sexually selected traits get elaborated, extinction
risk may be increased, for example by magnifying survival costs to males
(Promislow, 1992; Moen et al., 1999), or by causing gender load
associated with (partial) expression in females of alleles favoured by
sexual selection acting on males (Rice & Chippindale, 2001; Berger et
al., 2016).
Our results do not support the hypothesis that rate of extinction of
entire populations is increased because cost of developing and carrying
heavy weapons by males increase their mortality under environmental
challenge (Moen et al., 1999; Kokko & Brooks, 2003). Increasing
temperature did not disproportionately affect survival of males in FT
populations. Instead, in both FT and ST populations, females survived
better than males in early generations, but in generations 3 and 4 the
differences between the sexes disappeared, suggesting that female
survival was more negatively affected by increasing temperature compared
to males (Fig. S3). Our results support earlier suggestions that that
because of their widespread condition-dependence, elaborate sexually
selected traits should not compromise population fitness because most
males not express these costly traits when environment deteriorates
(Kokko & Brooks, 2003). This was indeed the case in the present study,
as proportion of fighters decreased across generations with increasing
temperature in FT populations, with proportion of fighters already down
to 75,7% at the first step of temperature increase (Figure S2). This
decrease can be explained by condition-dependence weapon expression
(Radwan, 1995; Smallegange, 2011; Plesnar-Bielak et al., 2018), and,
additionally by selection against ‘fighter genes’ under increased
temperature (Plesnar-Bielak et al., 2013). Irrespective of the cause,
suppression of weapon expression with increasing thermal stress did not
prevent extinctions. Indeed, most of extinctions occurred at generation
four, when only a minority (25%) of males expressed the costly weapon.
Thus, our results demonstrate that evolution of costly, sexually
selected traits may affect the risk of extinction even when the
expression of such traits is reduced due to their condition-dependence.
Thus overall, survival cost of developing and maintaining elaborated
sexual traits by males does not appear to be a reason for increased
extinction of FT populations. Another reason for elevated extinction
risk of fighter populations could be differences in effective population
sizes (Ne), which might occur if reproductive success among fighter
males is more biased compared to scrambler males. Parrett et al. (in
prep) have estimated Ne for populations fixed for scrambler and fighter
morph at 37% and 46% of the census population size, based on SNPs
frequency changes between generations. This implies that for our
populations of 50 individuals, Ne would be 18.5 and 23.0, respectively,
and the resulting increase in inbreeding over four generation, assuming
first generation was outbred, 0.08 and 0.10. A difference in inbreeding
of the order of 2% is unlikely to explain a significant proportion of
the difference in fitness and extinction risk between our treatments.
Yet another possible reason is increased sexual antagonism associated
with male weapon, which in the bulb mite was reported to be genetically
correlated with decreased female fecundity and survival (Plesnar-Bielak
et al., 2014; Łukasiewicz et al., 2020). Therefore, sexually
antagonistic, pleiotropic effects of male weapon on female fitness may
have contributed to increased extinction risk under genetic or
environmental stress. The role of ontogenetic conflict in extinction was
implied in the study of bean beetles, where inbred lines associated with
high male fitness, but low female fitness, suffered increased extinction
risk under inbreeding (Grieshop et al., 2017). However, that study did
not eliminate the possibility that high-male-fitness inbred lines
carried higher load of deleterious recessives. In case of our study,
such explanation could be ruled out by significantly lower inbreeding
depression we recorded in our fighter lines after four generations of
inbreeding (Łukasiewicz et al., 2020). The same study confirmed that
gender load was present, manifested as decreased fecundity in outbred
females descended from F-lines compared to those derived from S-lines.
This gender load may have interacted with environmental stress, thus
increasing extinction rate, as earlier suggested by Grieshop et al.
(2017) for genetic stress. Finally, F populations might have failed to
adapt to increasing temperature if deleterious variants removed from F
populations via enhanced “good genes” selection (Łukasiewicz et al.,
2020) were rendered adaptive under increased temperature (Jensen, 2014).
Further work is needed to discriminate between these alternatives.
It has been suggested that the increase in sexually selected dimorphism
may increase adaptive potential of populations by helping to maintain
genetic variance (Radwan et al., 2015) or by increasing environmental
scope (Bonduriansky, 2011; De Lisle & Rowe, 2015). Our results suggest
otherwise, but the outcome may be context-dependent and affected by e.g.
the rate of environmental deterioration and population size. Large
populations can better preserve genetic variation under negative
pleiotropy than small populations (Connallon & Clark, 2012), and thus
large populations of sexually dimorphic species may be able to use
sexually antagonistic variation to respond to environmental changes.
Furthermore, selection is more effective in larger populations, and
‘good genes’ effects may prevail over negative pleiotropic effects
(Martinez-Ruiz & Knell, 2017). Further work is required to elucidate
the role of costly, sexually selected trait on extinction at various
demographic and environmental scenarios.
Acknowledgements: We thank Joe Tomkins and Jon Parrett for
their comments on earlier versions of this manuscript, and Katerina
Altouva for help during experiments. This work was supported by NCN
grant UMO-2020/39/B/NZ8/00152to JR